Generalization indicates asymmetric and interactive control networks for multi-finger dexterous movements

Kamara, Gili; Rajchert, Ohad; Solomonow-Avnon, Deborah; Mawase, Firas

doi:10.1016/j.celrep.2023.112214

Cited by 6 publications

(1 citation statement)

References 62 publications

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“…A few studies that did test other movement directions in stroke-affected hands suggest differential impairment of finger independence in flexion, extension, and ad/abduction (Lang and Schieber 2003; 2004a). Moreover, studies that assessed naturalistic movements of the hand in healthy people have also shown that finger coactivation patterns can vary greatly depending on the tasks and fingers involved (Ingram et al 2008; Lang and Schieber 2004b; Todorov and Ghahramani 2004; Yan et al 2020), and that training finger individuation in the flexion direction does not transfer to the extension direction (Kamara et al 2023). Our recent finger flexion study (Xu et al 2017) suggests that finger individuation and strength follow different recovery processes and that they may be supported by different neural pathways, with individuation mainly supported by the corticospinal tract (CST) and strength largely driven by the reticulospinal tract (RST).…”

Section: Introductionmentioning

confidence: 99%

Loss of finger control complexity and intrusion of flexor biases are dissociable in finger individuation impairment after stroke

Xu,

Ma,

Kumar

et al. 2023

Preprint

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The ability to control each finger independently is an essential component of human hand dexterity. A common observation of hand function impairment after stroke is the loss of this finger individuation ability, often referred to as enslavement, i.e., the unwanted coactivation of non-intended fingers in individuated finger movements. In the previous literature, this impairment has been attributed to several factors, such as the loss of corticospinal drive, an intrusion of flexor synergy due to upregulations of the subcortical pathways, and/or biomechanical constraints. These factors may or may not be mutually exclusive and are often difficult to tease apart. It has also been suggested, based on a prevailing impression, that the intrusion of flexor synergy appears to be an exaggerated pattern of the involuntary coactivations of task-irrelevant fingers seen in a healthy hand, often referred to as a flexor bias. Most previous studies, however, were based on assessments of enslavement in a single dimension (i.e., finger flexion/extension) that coincide with the flexor bias, making it difficult to tease apart the other aforementioned factors. Here, we set out to closely examine the nature of individuated finger control and finger coactivation patterns in all dimensions. Using a novel measurement device and a 3D finger-individuation paradigm, we aim to tease apart the contributions of lower biomechanical, subcortical constraints, and top-down cortical control to these patterns in both healthy and stroke hands. For the first time, we assessed all five fingers' full capacity for individuation. Our results show that these patterns in the healthy and paretic hands present distinctly different shapes and magnitudes that are not influenced by biomechanical constraints. Those in the healthy hand presented larger angular distances that were dependent on top-down task goals, whereas those in the paretic hand presented larger Euclidean distances that arise from two dissociable factors: a loss of complexity in finger control and the dominance of an intrusion of flexor bias. These results suggest that finger individuation impairment after stroke is due to two dissociable factors: the loss of finger control complexity present in the healthy hand reflecting a top-down neural control strategy and an intrusion of flexor bias likely due to an upregulation of subcortical pathways. Our device and paradigm are demonstrated to be a promising tool to assess all aspects of the dexterous capacity of the hand.

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Section: Introductionmentioning

confidence: 99%

Loss of finger control complexity and intrusion of flexor biases are dissociable in finger individuation impairment after stroke

Xu,

Ma,

Kumar

et al. 2023

Preprint

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An ANN models cortical-subcortical interaction during post-stroke recovery of finger dexterity

Kadry,

Solomonow-Avnon,

Norman

et al. 2024

J. Neural Eng.

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Objective. Finger dexterity, and finger individuation in particular, is crucial for human movement, and disruptions due to brain injury can significantly impact quality of life. Understanding the neurological mechanisms responsible for recovery is vital for effective neurorehabilitation. This study explores the role of two key pathways in finger individuation: the corticospinal tract (CST) from the primary motor cortex and premotor areas, and the subcortical reticulospinal tract (RST) from the brainstem. We aimed to investigate how the cortical-reticular network reorganizes to aid recovery of finger dexterity following lesions in these areas. Approach. To provide a potential biologically plausible answer to this question, we developed an artificial neural network (ANN) to model the interaction between a premotor planning layer, a cortical layer with excitatory and inhibitory corticospinal outputs, and reticulospinal outputs controlling finger movements. The ANN was trained to simulate normal finger individuation and strength. A simulated stroke was then applied to the corticospinal (CS) area, reticulospinal (RS) area, or both, and the recovery of finger dexterity was analyzed. Main Results. In the intact model, the ANN demonstrated a near-linear relationship between the forces of instructed and uninstructed fingers, resembling human individuation patterns. Post-stroke simulations revealed that lesions in both CS and RS regions led to increased unintended force in uninstructed fingers, immediate weakening of instructed fingers, improved control during early recovery, and increased neural plasticity. Lesions in the CS region alone significantly impaired individuation, while RS lesions affected strength and to a lesser extent, individuation. The model also predicted the impact of stroke severity on finger individuation, highlighting the combined effects of CS and RS lesions. Significance. This model provides insights into the interactive role of cortical and subcortical regions in finger individuation. It suggests that recovery mechanisms involve reorganization of these networks, which may inform neurorehabilitation strategies.

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Direction-dependent neural control of finger dexterity in humans

Rajchert

Ofir-Geva

Melul

et al. 2023

Preprint

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Humans, more than all other species, skillfully flex and extend their fingers to perform delicate motor tasks. This unique dexterous ability is a product of the complex anatomical properties of the human hand and the neural mechanisms that control it. Yet, the neural basis that underlies human dexterous hand movement remains unclear. Here we characterized individuation (fine control) and strength (gross control) during flexion and extension finger movements, isolated the peripheral passive mechanical coupling component from the central neuromuscular activity involved in dexterity and then applied voxel-based lesion mapping in first-event sub-acute stroke patients to investigate the causal link between the neural substrates and the behavioral aspects of finger dexterity. We found substantial differences in dexterous behavior, favoring finger flexion over extension. These differences were not caused by peripheral factors but were rather driven by central origins. Lesion-symptom mapping identified a critical brain region for finger individuation within the primary sensory-motor cortex (M1, S1), the premotor cortex (PMC), and the corticospinal (CST) fibers that descend from them. Although there was a great deal of overlap between individuated flexion and extension, we were able to identify distinct areas within this region that were associated exclusively with finger flexion. This flexion-biased differential premotor and motor cortical organization was associated with the finger individuation component, but not with finger strength. Conversely, lesion mapping revealed slight extension-biases in finger strength within descending tracts of M1. From these results we propose a model that summarizes the distinctions between individuation and strength and between finger movement in flexion and extension, revealed in human manual dexterity.

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Generalization indicates asymmetric and interactive control networks for multi-finger dexterous movements

Cited by 6 publications

References 62 publications

Loss of finger control complexity and intrusion of flexor biases are dissociable in finger individuation impairment after stroke

Loss of finger control complexity and intrusion of flexor biases are dissociable in finger individuation impairment after stroke

An ANN models cortical-subcortical interaction during post-stroke recovery of finger dexterity

Direction-dependent neural control of finger dexterity in humans

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